2022 POLAR BEAR RESEARCH MASTERPLAN - Polar Bear Research Council Association of Zoos and Aquariums Polar Bear Species Survival Plan - Cincinnati ...
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
2022 POLAR BEAR RESEARCH MASTERPLAN Polar Bear Research Council Association of Zoos and Aquariums Polar Bear Species Survival Plan
This publication may be cited as: Polar Bear Research Council. 2022. 2022 Polar Bear Research Masterplan. Polar Bear Species Survival Program, Association of Zoos and Aquariums. On the cover: Polar bear Tasul swims into an underwater swim flume as part of a collaborative metabolic study at the Oregon Zoo. Photo by Michael Durham/Oregon Zoo.
Table of Contents AZA Polar Bear SSP Research Council . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 List of PBRC endorsed, ongoing research projects as of June 2021 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 Field Techniques . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8 Health and Welfare . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 Physiological and Behavioral Ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16 Reproduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 Dr. Anthony Pagano records behavior exhibited by Oregon Zoo polar bear Tasul, voluntarily sporting a research collar fitted with an accelerometer device. Photo by Michael Durham/Oregon Zoo.
O ver the past 40+ years, scientists have overcome tremendous logistical challenges to study wild polar bears, and I feel fortunate for the role I’ve played in that progress. Prior to joining Polar Bears International as chief scientist in 2010, I led polar bear research in Alaska for 30 years. My three decades of in situ fieldwork helped provide essential information on polar bear movements, distribution, population trends, life history traits, and basic biological needs—knowledge that has added greatly to our understanding of the bears and the actions needed to ensure their future. This research culminated in the projection that, without action on human-caused climate warming, polar bears could all but disappear by the end of the century. As a result, polar bears became the first species listed under the U.S. Endangered Species Act due to the threat of global warming. Dr. Steven C. Amstrup Continuing in situ research on wild polar bears across the Arctic has confirmed the threat of climate warming and provided the mechanistic underpinnings of polar bear life history needs. It also has shown that some vital studies simply cannot be conducted in the wild. This is where zoos and aquariums can play a critical role. Bears in managed care can be repeatedly observed and sampled over long time periods—allowing sample size and replication not possible in the field. Such studies can fill critical knowledge gaps while testing and calibrating new research methods and technologies before they are deployed in the field. Through projects supported by the Polar Bear Research Council, of the Association of Zoos and Aquariums, AZA member institutions have partnered with universities, government agencies, and Polar Bears International on research ranging from determining the polar bear’s energy use when walking, running, and swimming to testing new devices for following the movements of bears in the wild. Ex situ research in zoo settings combined with in situ field research showed how polar bears use scent communication as they search for mates on broad expanses of pack ice. And studying polar bear hair and tissue samples from zoo animals have helped us understand wild bear diets. The Polar Bear Research Masterplan is a living document that prioritizes ex situ research vital to polar bear conservation and management. It serves as a roadmap to the roles zoos and aquariums can fill in our understanding of polar bear life history needs. Presentation of ex situ research also can capture public attention and enhance the opportunities for zoos and aquariums to educate the public about the threats polar bears face—inspiring actions necessary to preserve them in the wild. The combination of ex situ research opportunity with potential for outreach and education means zoos and aquariums can play a vital role in helping to assure future survival of polar bears throughout the Arctic. This document is a valuable resource for guiding, facilitating, and supporting this important work. Sincerely, Dr. Steven C. Amstrup Chief Scientist, Polar Bears International 4 | PRBC Masterplan 2022
Mission: To ensure a robust, thriving zoo population The Polar Bear Research Council (PBRC) of polar bears is involved in research that produces solutions to conservation and management challenges facing wild bears. T he PBRC is composed of a Steering Committee that includes two PBRC Co-Chairs, the PBRC Facilitator and the Polar Bear SSP Chair. Additional members Description: The Polar Bear SSP’s designation as a include advisors with expertise/experience in four research population signals a shift toward requiring priority research areas (see below). Priority research member participation in priority research projects advisors are responsible for recruiting input from with polar bears ex situ that can inform critical additional experts (typically 3-6) who can provide conservation and management questions that exist thoughtful reviews and unique perspectives to ensure for polar bears in situ. For a research program to be the PBRC Masterplan is accomplished. successful, a diverse population of animals must be The PBRC’s goals are to: 1) facilitate the use of the ex situ maintained, individual animal welfare must factor population to better characterize basic biology and to into decision-making and AZA facilities must work to advance scientific methodologies for comparison and ensure that viable candidates are available for research. application to wild polar bears; 2) support research that Additionally, AZA facilities must ensure that staff are is necessary for maintaining a viable, sustainable ex trained in sample collection and training techniques, situ population for scientific research with application and that facilities are designed to accommodate to the conservation of wild bears; and 3) build capacity sample collection and/or research. Future polar bear within SSP member institutions to participate in priority SSP master-planning will center around maximizing scientific research efforts. our participation in meaningful conservation science. Rationale: Polar bears in managed care can Purpose of the PBRC and the Research Masterplan T participate in valuable research that helps to conserve he purpose of the Polar Bear SSP Research and understand polar bears in the wild. Zoo- and Masterplan document is to: 1) guide research aquarium-housed polar bears can be trained via priorities for the Polar Bear SSP and participating operant conditioning to voluntarily participate in institutions, 2) advise the Polar Bear SSP on proposal hands-on procedures and longitudinal biological endorsement requests, 3) facilitate priority research sampling. These bears have the added advantage in efforts in SSP institutions, 4) keep current with that their husbandry histories and medical records are emerging scientific questions regarding survival of available, environmental conditions are known and can polar bears in the wild, and 5) track progress made be adjusted, and monitoring can be continuous during through the collaborative scientific studies of polar a study. Through multi-institutional collaborations, bears in managed care and of contributions made scientists can recruit a larger sample size of polar by zoos and aquaria to wild polar bear research. The bears that ensure sufficient statistical power in masterplan is a living document that is intended to studies on behavior, physiology, health, reproduction, be updated every three to five years. This current and welfare. Polar bears in managed care can also masterplan is the 1st revised version of the original contribute to the development and validation of new masterplan published in 2018. technologies and methodologies for use with wild bears, the true beneficiaries of this initiative. Photo © Daniel J. Cox/NaturalExposures.com PRBC Masterplan 2022 | 5
AZA Polar Bear SSP Research Council Co-Chairs Priority research pillars and corresponding advisors Dr. Terri Roth, Center for Conservation and Research of Endangered Wildlife (CREW), Cincinnati I. Field Techniques Advisors Zoo & Botanical Garden; email: terri.roth@ cincinnatizoo.org Dr. Thea Bechshoft, Polar Bears International; email: thea@pbears.org Dr. Megan Owen, San Diego Zoo Wildlife Alliance; email: mowen@sdzwa.org Dr. Stephen Petersen, Assiniboine Park Zoo; email: spetersen@assiniboinepark.ca Facilitator and Contact: Amy Cutting, Oregon Zoo; II. Health and Welfare Advisor email (preferred) Amy.Cutting@oregonzoo.org; Dr. Randi Meyerson; email: randimeyerson61@ cell: 503-757-8163; Office: 503-220-2446 gmail.com AZA Liaison: Steve Olson, Senior Vice President, Government Affairs, Association of Zoos and III. Physiological and Behavioral Ecology Advisors Aquariums (AZA); email: solson@aza.org Dr. Karyn Rode, United States Geological Survey Polar Bear SSP Chair: Allison Jungheim, Como Park (USGS); email: krode@usgs.gov Zoo and Conservatory; email: allison.jungheim@ Dr. Anthony Pagano, Washington State ci.stpaul.mn.us University; email: ampagano@ucsc.edu IV. Reproductive Physiology Advisor Dr. Erin Curry, CREW, Cincinnati Zoo & Botanical Garden; email: erin.curry@cincinnatizoo.org 6 | PRBC Masterplan 2022
List of PBRC endorsed, ongoing research projects as of June 2021 Project title PI and affiliation 1 Macronutrient requirements and intake of Karyn Rode; USGS; krode@usgs.gov polar bears 2 Comparative analyses of the Shannon Atkinson and Monica Brandhuber; expression of reproductive steroids and University Fairbanks; shannon.atkinson@ dehydroepiandrosterone sulfate (DHEAS) in alaska.edu captive and wild female polar bears. 3 Characterization of the gut microbiota in Peko Tsuji and Maci Quintanilla; Towson polar bears and a metabolic analysis University, MD; ptsuji@towson.edu 4 Development of dynamic energy budget Stephanie Penk; University of Toronto; models in complex vertebrate mammals sr.penk@mail.utoronto.ca to understand past and future population dynamics. 5 Validation and characterization of Erin Curry, Jessye Wojtusik, Terri Roth; reproductive hormones and biomarkers Cincinnati Zoo/CREW; erin.curry@ in polar bear serum cincinnatizoo.org 6 Analyzing hormone patterns of captive Dylan McCart, Suzanne MacDonald; York male polar bears housed under different University; dylanmccart@hotmail.com social conditions 7 Assessing the timing and rate of fur Jennifer Stern, University of Washington growth in zoo polar bears and Karyn Rode, USGS; jhstern@uw.edu 8 Polar bear ear measurements (for new Elisabeth Kruger; World Wildlife Fund; ear tag tracking device) Elisabeth.Kruger@wwfus.org 9 Serum concentration comparisons of fatty Deb Schmidt, St. Louis Zoo and Karyn Rode, acids, amino acids, vitamins, minerals, and USGS; schmidt@stlzoo.org cholesterol, between free-ranging and zoo polar bears 10 New attachment techniques for electronics Geoff York, Polar Bears International; to polar bears – Project “Burr on Fur” gyork@pbears.org PRBC Masterplan 2022 | 7
FIELD TECHNIQUES Field Techniques (In-field monitoring and management techniques) Advisors: Dr. Thea Bechshoft, Polar Bears International Dr. Stephen Petersen, Assiniboine Park Zoo Experts: BJ Kirschhoffer, Polar Bears International Liz Larson, Utah’s Hogle Zoo Alysa McCall, Polar Bears International Dr. Nicholas Pilfold, San Diego Zoo Wildlife Alliance Dr. Tom Smith, Brigham Young University Geoff York, Polar Bears International Explanation of the research focus area in relation to polar bear conservation The polar bear (Ursus maritimus) poses challenges for researchers and conservationists in that it is a large top predator that lives a primarily solitary life across vast expanses in a harsh and remote environment. Polar bear habitat also presents logistical difficulties and safety concerns for researchers as it consists of sea ice, marine waters, and terrestrial areas that experience a wide range of often unforgiving environmental Photo © Daniel J. Cox/NaturalExposures.com conditions. When polar bears do occur near humans and their infrastructure successfully co-existing can will provide the desired data and results. An additional present a significant risk and challenge. Together, benefit is that the newly developed methods are often these factors often hinder effective research and less invasive than the more traditional approaches to conservation efforts of polar bears across the Arctic. polar bear research. Technical and technological advances can play a vital role in overcoming this challenge, particularly The Field Techniques advisory group includes projects those that have been developed in collaboration with with direct in-field applications, in particular studies institutions that have polar bears in their care. These that test equipment for field deployment or validate bears can participate in scientific studies in a controlled new (or new applications of already existing) methods environment, with subjects that can be repeatedly and technologies that directly inform in situ polar bear observed, monitored, or examined. Thus, applied research and conservation. Meanwhile, projects focused monitoring and conservation tools that have been on advances in laboratory analyses and techniques developed using ex situ bears can be nearly field-ready will sort under either the Physiological and Behavioral before being deployed in situ, reducing the chance of Ecology, the Reproductive Physiology, or the Health and failure, and increasing the chances that field results Welfare advisory groups as deemed appropriate. 8 | PRBC Masterplan 2022
FIELD TECHNIQUES Recent examples of published work that has happened in zoo settings and how it has complemented or informed our understanding of polar bear biology and management Identifying bear behavior from activity sensors Pagano et al. (2017) and Ware et al. (2016) used activity sensor data on collars of zoo bears to relate collar activity to individual bear behaviors. Those relationships have then been used to be able to identify the behaviors of wild bears our on the sea ice based on historic and contemporary activity sensor data thereby better understanding the behavior of bears when and where they can rarely be observed. Energetic costs of locomotion in bears Infrared thermography image of a male polar bear. Pagano et al. (2018a) - Polar bears in human care were Image by Dylan McCart and Dr. Michelle Shero. trained to voluntarily walk on a treadmill in a special chamber that could analyze the breath of the bear. their blood and hair. Using this information, correction This allowed scientists to record how the bear was factors were identified that allow estimation of the moving at as well as the amount of energy they were prey species and macronutrient composition of wild expending. This information was then used to predict polar bear diets from these same tissues. Further, this energy use in wild bears. study determined the timeframe of diet represented in these tissues to improve interpretation of wild samples. Identification of individual bears Prop et al. (2020) - Sets of photographs of 15 polar Priority areas that should take precedence bears from six AZA and EAZA zoos were used to within this research pillar develop a new method for individual recognition, Given the unpredictable nature of methodological based on distinguishing a set of physiognomic and technological advances, we have identified characteristics, which can be recognized from priority areas where new field techniques are likely photographs taken in the field at distances of up to 400 m. Requiring less specific photos than the whisker to contribute significantly to our understanding and spot recognition method (Anderson et al. 2010), conservation of polar bears. this new method offers an additional method for 1. Population assessment: The key to managing identification of individual polar bears in the wild. populations is obtaining regular and timely population estimates to determine abundance and Validating thermal imagery tools trends. For polar bears, this has been accomplished Bissonette (2020) - Polar bears in human care were using capture-mark-recapture (hands-on and filmed using an infrared camera while the bears sparred genetic) and via aerial surveys. All current methods and played with each other. The change in the bear’s are expensive, high risk, and time-consuming temperature signal from beginning of the play session and therefore cannot be done with the regularity to the end of a session is related to the amount of needed for a species in a changing habitat such as energy the bear has spent on that activity. Thermal the Arctic. Examples of emerging technology likely imagery has been used to detect polar bear dens (Smith to assist in counting polar bears include remote et al. 2020) but may also have other applications to help sensing tools that could help us accurately count understand polar bear biology and behaviour. bears using drones, aircraft, or satellites (e.g., LaRue et al. 2015, Barnas et al. 2018). Improving diet estimates of wild polar bears inferred from hair and blood samples 2. Movement and dispersal: Habitat use and Rode et al. (2016) worked with zoos to feed polar requirements, movement, and dispersal studies bears specific marine-based diets to trace how stable all rely on the tracking of individual polar bears. isotopes of carbon and nitrogen in food is reflected in This has been done primarily using satellite- PRBC Masterplan 2022 | 9
FIELD TECHNIQUES GPS ear tag on a tranquilized subadult polar bear. Photo by Dr. Andrew E. Derocher/ University of Alberta. onshore and as human activities in the Arctic increase, both in response to longer ice-free seasons (Wilder et al. 2017). To mitigate this, more information is needed on polar bear olfaction and vision in relation to potential deterrent tools and methods. Further, development and testing of early polar bear detection systems as well as non-harmful deterrent tools such as strobe linked GPS collars, but there is an increasing lighting and specific sounds to examine their need for redesign of these instruments to be efficacy in potential use as a deterrent option. smaller, lighter, and more efficient. There is also a need for them to be able to carry new sensors 5. Polar bear awareness: Human perceptions of polar or be attached in different ways. Examples of bears and their actions can significantly influence emerging technology likely to assist in tracking chances of human/bear conflict when working, polar bears include miniaturization and new living, or recreating in the north. Social science battery technology as well as new tracking device research that probes this relationship and explores attachment strategies like the one used in the 3M ways to minimize conflict is needed. Burr on Fur adhesive tags. A prototype of one of the Burr on Fur adhesive GPS tags. 3. Minimally invasive monitoring: Devices like As with the ear tags, these smaller tags allow us to study camera traps, Doppler tracking radar, hair snags, not just adult females, but also males and younger photogrammetric or laser-based body condition bears, collecting valuable information on the habitat measures, and opportunistic collection of fecal use of these little-studied groups. Photo by 3M and Polar samples are good examples of non-invasive Bears International. monitoring tools. Approaches like these can provide useful information on polar bears with minimal disturbance or effect on the animal. Non- or minimally invasive techniques should be pursued and used whenever possible over invasive techniques and can be tested and validated in zoological or aquarium settings. 4. Polar bear/human coexistence: Sea ice loss has led to an increase in polar bear sightings in northern coastal communities around the Arctic, a trend that is expected to continue as more polar bears are forced to spend longer periods of time 10 | PRBC Masterplan 2022
FIELD TECHNIQUES Work currently underway or not yet published o Body condition; developing an algorithm that allows body condition to be inferred 1. Population assessment from photographs or laser-based three- dimensional imagery. o Collection of aerial thermal images of polar bears to train machine learning algorithms to o Individual recognition; further development detect polar bears in seal surveys. of the automated system developed by the Waterman group (Anderson et al. 2010) that 2. Movement and dispersal uses whisker spot patterns to identify bears. o Testing of adhesive satellite tags that attach to 4. Polar bear/human coexistence the bear’s fur while providing movement data. o Ear tag redesign for a smaller more ergonomic o Early warning polar bear detection; developing tag to replace the current bulkier design. a radar technology based system to reduce human-polar bear conflict in remote locations. 3. Minimally invasive monitoring o Polar bear olfactory preferences; assessing a range of scents for their properties as potential o SAR (synthetic aperture radar); a device used attractants/deterrents. to detect polar bear maternity dens under the snow while flying overhead. 5. Improving methods for studying polar bear o Maternal den studies; monitoring polar bear ecology from tissue samples dens with remote camera systems to record data on the activity of emerging polar bear o Assessing the timing and rate of fur growth moms and cubs. in zoo polar bears to improve interpretation of studies of diet, contaminants, and stress hormones in fur. Polar bear Nora swims in a metabolic chamber as part of an energetics study at the Oregon Zoo. Photo by Michael Durham/Oregon Zoo. PRBC Masterplan 2022 | 11
HEALTH AND WELFARE Health and Welfare Advisor: Dr. Randi Meyerson Experts: Dr. Dalen Agnew, Michigan State University Dr. Todd Atwood, USGS Dr. Jonathon Cracknell, European Association of Zoos and Aquaria Dr. Wynona Shellabarger, Detroit Zoological Society Dr. Patricia Pesavento, University of California, Davis Explanation of the research focus area in relation to polar bear conservation The Veterinary Medicine Research subcommittee identified health and welfare concerns of wild and zoo managed polar bears, trends in pathology, and the threat of emerging diseases in a warming Arctic as their top priorities. Though the greatest threat to polar bears is loss of sea ice, disease related factors were identified as important criteria both for their 2008 listing under the Endangered Species Act (USFWS, 2008) and for recovery in the 2016 USFWS Polar Bear Conservation Management Plan (USFWS, 2016). Photo © Daniel J. Cox/NaturalExposures.com A warming and changing Arctic environment is having significant effects on wild polar bears. Shorter annual While types of impact, such as starvation, decreased periods of sea ice availability, with corresponding reproduction and immune function, and increased shorter periods of time for bears to hunt ice seals, susceptibility to disease are easy to predict; studies has been associated with declines in body condition, of the S. Beaufort Sea polar bears demonstrate that reproductive success, survival, and abundance. the specific effects on the differing subpopulations Poor body condition decreases immune function, are not. Differing lengths of time on shore, types and making the bears more susceptible to pathogens, levels of food source availability, and prior exposure as well as the effects of fat-soluble contaminants, to pathogens were all shown to have significant effect as their fat supplies become depleted. Additionally, on the health status of individual bears (Atwood et.al a warming environment, with a greater ice-free 2017; Neuman-Lee et. al 2017). period, increases exposure to infectious diseases, both through increased concentration of conspecifics While a major focus of the polar bear research and other species affiliated with human settlements, masterplan is to facilitate ex situ research to help as well as northern migration of novel pathogens answer in situ questions, the plan also prioritizes the and vectors (Fagre et al., 2015). As the loss of sea ice need to continue addressing the health and welfare continues unabated, greater exposure to pathogens concerns of the zoo managed polar bear population. and parasites has the potential to adversely affect the health of the polar bear populations. 12 | PRBC Masterplan 2022
HEALTH AND WELFARE Male polar bear anesthetized for physical examination. Photo by Louisville Zoo. Examples of work that has happened in zoo Pathogenic studies settings and how it has complemented or informed Bears in our care, with known health histories, exposure locations and the ability to provide our understanding of polar bear biology and sequential blood samples can provide information management related to pathogenic titers (Neuman-Lee et al., 2017; Dutton et al., 2009). Study results have shined Gene transcription studies a light on the large number of factors that must be Studies of gene transcription have been conducted considered in interpreting results. to assess ecological and anthropological stressors (Bowen et.al, 2015). Results revealed immune function impairment in polar bears from the Beaufort Sea, when Research Priority Areas compared with Chukchi and captive polar bears. Given the expanse of the study of polar bear health, many of the issues identified in this section of the Feeding trials document will also be included in other areas of the Polar Bear Research Masterplan. Studies involving closely monitored feeding trials have been performed to quantify dietary lipid and Additionally, this section not only looks at veterinary protein preference in zoo bears, and data have been issues involving wild polar bears, but the health and compared with that from studies of wild bear diets to welfare of bears in human care as well. It is essential infer optimal macronutrient intake (Rode et al., 2021). that zoo bears are healthy both mentally and physically Results indicate that bears should consume more lipid and display many natural behaviors so that research and less protein than previously thought. results are transferable to wild bears. PRBC Masterplan 2022 | 13
HEALTH AND WELFARE 1. Veterinary health and welfare: Although zoos o Investigate the polar bears’ ability to adapt to have greatly improved their facilities and care higher thermal temperatures. of bears over the years, managed polar bears continue to face several challenges that may have o Identify and address behavioral and an impact on their welfare. The success of the physiological causative and indicators of stress. managed population depends on each individual bear’s ability to thrive. Therefore, identifying factors 2. Pathology in the physical and social environments that o Establish/centralize tissue and plasma banks in contribute to positive welfare is critical. In addition US and Canada to being an important conservation education ambassador for climate change, these bears, as o Establish consistent necropsy protocols participants in conservation relevant research, for field and zoo use which facilitate afford the opportunity to better understand how collaborations and comparisons between current and future environmental changes and zoo managed and wild polar bears. Including challenges are affecting or will affect their wild “how to” photographic documentation, populations as well. Whereas, some areas of study morphometrics, and the creation of a are specific to their wild or captive status, other brief instructional video for necropsy studies have relevance to both populations. procedures for field biologists. o Investigate poor captive reproductive success. o Coordinate retrospective and prospective necropsy data. o Develop effective hand-rearing protocols. o Standardize sampling techniques in the field o Define effective care and management for and zoos in relation to histology, cytology, geriatric bears. virology, toxicology, parasitology, biotoxins, o Identify common dermatological issues and and genetics studies. possible relationships to nutritional status, immune function, reproductive status, and/or water quality. Voluntary blood collection from a polar bear. Photo by Como Park Zoo & Conservatory. 14 | PRBC Masterplan 2022
HEALTH AND WELFARE o Establish baseline assessment of infectious disease burden. o Establish baseline characterizations of the microbiome and virome. 4. Technological Advancements for Healthcare o Establish a protocol for indicators/measures of stress- i.e. voluntary blood draw sampling of consecutive cortisol levels after periods of stress to help determine delay period between stressor and blood/fecal/hair cortisol level changes. o Development of techniques that permit oiled/ ill/injured bears to be treated in situ and/or in close proximity to their natural territory and associated sub-populations. o Optimize techniques and training of polar bears for minimally invasive sampling and veterinary treatments. Studies currently underway or not yet published 1. Evaluation and comparison of Toxoplasmosis gondii titers in wild and zoo polar bears and Polar bear cub CT scan as part of neurological exam. implications to the health of the polar bears Photo by Wynona Shellabarger/Detroit Zoological Society. and the Inupiat communities that harvest them. R. Meyerson and W. Shellabarger, Detroit Zoological Society. 3. Emerging diseases 2. Investigating the relationship between ambient o Evaluate potential emerging diseases from conditions and thermoregulatory responses vector migration northward as habitat warms- in polar bears. L. Graham, WRG Conservation i.e. mosquitoes and West Nile Virus Foundation and Ryerson University. o Evaluate disease concerns in their prey species; 3. Multi-institutional evaluation of peri-vulvar both availability and possible cross-species dermatitis in female polar bears and implications transmission. to welfare and health concerns in both zoo and wild bears. E. Curry, Center for Conservation and o Evaluate increased exposure at the human Research of Endangered Wildlife, W. Shellabarger, interface to infectious disease carriers, such as Detroit Zoological Society. domestic dogs and cats, as polar bears seek out human food caches, and humans move 4. West Nile titers in zoo polar bears as indicators into or spend greater amounts of time in more of threat to wild polar bears in a warming northern latitudes Arctic. R. Meyerson and W. Shellabarger, Detroit Zoological Society. o Evaluate increased exposure to novel species as a sequela to warming (isolation, migration) or translocation (zoos) PRBC Masterplan 2022 | 15
PHYSIOLOGICAL AND BEHAVIORAL ECOLOGY Physiological and Behavioral Ecology Advisors: Dr. Karyn Rode, USGS Dr. Anthony Pagano, Washington State University Experts: Dr. Thea Bechshoft, Polar Bears International Dr. John Whiteman, Old Dominion University Dr. Tom Smith, Brigham Young University Explanation of the research focus area in relation to polar bear conservation Understanding the mechanisms by which the current and near-future status of polar bears will be affected by sea ice loss and other ecosystem changes associated with climate change is important for informing management decisions and improving the accuracy of long-term projections. Although information on Photo © Daniel J. Cox/NaturalExposures.com population abundance and trends are critical, for most polar bear populations the logistical limitations of gathering data from a species that occupies a very Examples of work that has happened in zoo large home range throughout remote regions of the settings and how it has complemented or Arctic precludes estimation of population parameters. informed our understanding of polar bear Thus, management decisions often must be made based on inference of population dynamics based biology and management on bear health, nutritional condition, behavior, and In recent years, a number of studies of polar bear ecology. Further, as sea ice loss has become the physiological and behavioral ecology have been primary threat facing polar bears, there is an increased conducted in zoos, with findings being applied to better need to understand mechanistic relationships understanding polar bears in the wild. These include: between sea ice loss and polar bear population dynamics to improve short-term and long-term Validation of activity sensors projections. Thus, increasingly polar bear studies have Validation of activity sensors in collars for identifying focused on understanding behavioral responses to sea polar bear behavior including differentiating ice loss and physiological limitations in their ability to resting versus active behavior from archived polar adapt. To accommodate those studies, new methods bear activity sensor data (Ware et al. 2015; 2017) are needed. Polar bears in zoos provide an excellent and classifying swimming, walking, and resting opportunity for development of new methods to behavior using more recently developed tri-axial monitor polar bear behavior and physiology in the wild accelerometers (Pagano et al. 2017). and to better understand the physiological limitations of the species. Quantifying stable isotopes Quantifying routing of stable isotopes in polar bear diets into tissues to use samples of polar bear blood and hair from wild polar bears to estimate diets (Rode et al. 16 | PRBC Masterplan 2022
PHYSIOLOGICAL AND BEHAVIORAL ECOLOGY 2016). This information will allow detection of dietary Chemical communication changes over time that may be associated with sea Studying polar bear chemical communication to better ice loss or other environmental changes. Because diet understand social behavior, including breeding (Owen can affect exposure to contaminants and pathogens et al. 2015). Little has been known about how polar (McKinney et al. 2009, 2017), dietary change is an bears communicate and maintain social relationships important component of understanding potential out on the sea ice. Habitat fragmentation associated cumulative effects of ecological change. with sea ice has been identified as a potential factor that could disrupt breeding behavior in the spring. This Measuring metabolic rates study provided baseline information needed in better Measuring metabolic rates of polar bears while understanding potential implications of changing walking and swimming (Pagano et al. 2018 b, c). habitat conditions on social interactions. This information is important to understanding the energetic costs of behavioral changes and variation Hearing sensitivity in polar bears in polar bears. For example, polar bears have been Concerns regarding the spatial and temporal overlap documented to increasingly swim long distances in of oil and gas activities and maternal denning on the southern Beaufort Sea during the annual sea ice Alaska’s North Slope led to initiation of a studying minimum (Pagano et al. 2012). Additionally, changes of hearing sensitivity in polar bears. These baseline in patterns of sea ice drift have been shown to increase data (Owen & Bowles 2011) can be used to develop the rate of walking polar bears must maintain to travel biologically relevant protective guidelines for (Durner et al. 2017). Data on metabolic rates will allow industrial/human activity in sensitive polar bear quantification of the impacts of such changes. habitat (Owen et al. 2021) Female polar bear Tatqiq swimming in her pool at the San Diego Zoo while participating in a study designed to validate collar-mounted activity sensor data. This study, co-led by USGS and the UCSC, contributed to the behavioral classification of data generated by both tri-axial accelerometers and mercury tip-switch sensors. Photo by San Diego Wildlife Alliance. PRBC Masterplan 2022 | 17
PHYSIOLOGICAL AND BEHAVIORAL ECOLOGY Priority areas that should take precedence within this research area While it is difficult to foresee the variety of ways polar bears in zoos could help to better understand the behavioral and physiological ecology of polar bears, some recent themes have emerged as important contributions that could be made in the coming years. 1. Improve and validate methods for monitoring exposure to stressors and the state of chronic stress via cortisol in hair and urine or other metrics from blood. 2. Identify the seasonal timing of hair growth and rates of growth and the factors that affect these metrics, such as food intake, nutritional condition, size, age, sex, and environmental conditions in order to improve use of hair as an ecological monitoring tool for wild polar bears. 3. Continue to improve estimation of energetic costs in polar bears including identifying the primary factors affecting these costs, such as sex, age, and environmental conditions. These efforts should include quantification of the energetic costs of reproduction, lactation, and growth. Columbus Zoo bear sniffing meat in feeding trial. 4. Develop a detailed understanding of social Photo by Devon Sabo. communication in polar bears and determine how rapid environmental change may compromise mate search, courtship, social spacing and 7. Describe the range of maternal care behaviors that maternal care. are correlated with successful cub rearing. 5. Identifying stimuli to both attract and deter Work currently proposed, underway or polar bears. Attractants would be invaluable not yet published for improving capture rates for hair sampling devices. Studies of deterrents may be invaluable Several studies are currently underway, including for improving co-existence for human activities in a study of hair growth rates, a comparison of polar bear habitat. micronutrients in polar bear serum between wild and zoo bears, an evaluation of optimal dietary 6. Better understand macro and micronutrient macronutrient ratios, estimation of stable isotope requirements, including relationships between discrimination in the lipid and protein components intake and weight gain, in order to better of blood serum, and a study of bear behavior for understand implications of changing diets. improving hair collection. 18 | PRBC Masterplan 2022
REPRODUCTION Reproduction Advisor: Dr. Erin Curry, CREW, Cincinnati Zoo & Botanical Garden Experts: Dr. Laura Graham, Ryerson University Dr. Gaby Mastromonaco, Toronto Zoo Dr. Justine O’Brien, Taronga Conservation Society Australia Dr. Terri Roth, CREW, Cincinnati Zoo & Botanical Garden Explanation of the research focus area in relation to polar bear conservation Photo © Daniel J. Cox/NaturalExposures.com A reduction in the availability of Arctic sea ice upon which polar bears hunt is resulting in decreased female samples can be collected regularly from the ex situ body weights (Stirling et al. 1999; Rode et al. 2010; population, the concentrations and fluctuations Obbard et al. 2016), is predicted to result in increased of specific hormones and biomarkers can be reproductive intervals (Derocher and Stirling, 1994), characterized in controlled settings and throughout and to negatively impact litter sizes (Molnar et al. the lifetime of an individual, an impossible endeavor 2011). Reproductive success is essential to species when considering the wild population. Information survival, and reduced fecundity is often a precursor gained from studying zoo bears may allow for more to a population’s decline. Given the impending crisis accurate assessments of the reproductive physiology facing wild bears, the advancement of reproductive of wild populations and may provide insights into monitoring techniques will provide enhanced how variables such as body condition, environmental methodologies necessary to better determine how the contaminants, and human disturbances may impact species is coping with the changing environment. reproductive processes of in situ populations. Anthropogenic impact, such as human-induced Examples of work that has happened in zoo climate change and environmental contaminants, settings and how it has complemented or may impact fertility of polar bears, but the ability to assess the intricacies of reproduction in this species is informed our understanding of polar bear hindered by a lack of monitoring methods. In females, biology and management there is no established technique for diagnosing A growing number of reports have stemmed from pregnancy or distinguishing true pregnancy research of the ex situ population and have provided from pseudo-pregnancy; therefore, frequency of insight into the medley of reproductive phenomena pregnancy loss cannot be determined. In males, experienced by this species: there are challenges associated with the collection of semen, so knowledge of baseline gamete biology Non-invasive monitoring methods to better is deficient. The zoo managed population of polar characterize reproductive processes bears provides valuable opportunities to develop Fecal and urine progesterone and testosterone improved monitoring approaches that may enhance metabolite analyses have yielded understanding our understanding of how various factors impact of ovarian activity, including timing of ovulation the reproductive physiology of wild bears. Because and re-activation of the corpus luteum in females PRBC Masterplan 2022 | 19
REPRODUCTION An ultrasound examination is conducted on an anesthetized female polar bear. Photo by Seneca Park Zoo. that have bred. Progestogen analysis of females on which he was trained, but he failed to generalize to which were housed without males or with non- novel pregnancies. Fecal testosterone analysis showed intact males has provided verification that true that testosterone concentrations are significantly pseudopregnancy does exist in this species (Stoops higher during the breeding season and that males et al., 2012, Steinman et al., 2017, Knott et al., 2017) housed with females exhibit higher testosterone and indicates that progesterone concentrations alone than those housed without females, indicating that cannot be used to infer pregnancy status. Seasonal testosterone concentrations may be influenced by the and reproductive impact on fecal glucocorticoid (FGC) presence of sexually mature females (Curry et al., 2012). excretion was studied in a small group of pregnant and pseudopregnant bears (Bryant and Roth, 2018). Defining breeding season and assessing Glucocorticoid patterns varied among individuals reproductive behaviors and were not consistent within pregnancy status An investigation of multi-institutional records has or across seasons. Fecal protein analyses indicated that the concentrations of specific proteins and defined the polar bear breeding and cubbing seasons: protein fragments may be significantly higher in 85% of matings occurs between 12 February and 8 April pregnant versus pseudo-pregnant females (Curry et (Curry et al., 2012) and 74% of litters were born between al., 2012); however, additional research is needed to 13 November and 15 December, with mean and median determine if fecal proteins may provide an accurate, litter birth dates of 29 November (Curry et al., 2015). reliable pregnancy test. Similarly, in a study aimed to Because entire mating bouts are difficult to observe, and determine if odor detection dogs could distinguish the precise day of parturition is unknown in wild bears, fecal samples originating from pregnant versus non- detailed descriptions of breeding and parturition dates pregnant polar bears (Curry et al., 2021), the dog in zoos may be useful in characterizing the reproductive alerted on novel samples collected from pregnancies seasonality of this species. 20 | PRBC Masterplan 2022
REPRODUCTION Semen collection and cryopreservation Performing urethral catheterization in males anesthetized with medetomidine results in a sperm recovery rate of 87% in the breeding season and 30% in the non-breeding season (Wojtusik (in prep), Curry 2016 and 2017). These methods are field-friendly and potentially could be used to assess sperm parameters of wild bears while also providing valuable genetic material for long-term storage. The effects of various semen extenders and sperm cryopreservation methods are being studied, and a polar bear sperm bank has been established. Current cryopreservation methodologies result in a post-thaw sperm motility rate of up to 60% (unpublished; CREW). Priority areas that should take precedence within this research pillar The reproduction research priorities are focused on three strategies which are in alignment with the Polar Bear Research Council’s mission: 1) Use the ex situ population to better characterize basic reproductive physiology and improve monitoring techniques for comparison and application to in situ polar bears; 2) conduct research that is necessary for maintaining a viable, sustainable ex situ population for scientific research with application to wild bears; and 3) preserve the extant gene pool to prevent loss of genetic diversity Polar bear sperm. Photo by Cincinnati Zoo & Botanical that could occur due to environmental changes. Garden. 1. Improve and expand reproductive monitoring behaviors. Identifying factors or management capabilities: Although fecal steroid metabolite strategies among individuals and institutions analysis provides insight into reproductive that experience reproductive success may allow processes, no definitive diagnostic indicators predictions to be made on potential causes of of ovarian activity and pregnancy have been reproductive failure in wild bears. Maintaining a validated. Efforts should be made to further viable ex situ population is essential in serving investigate non-invasive (feces, urine, saliva, other) a wide range of conservation-relevant research and minimally invasive (serum) biological matrices needs, but currently, the ex situ population is and novel approaches to expand and improve not self-sustaining due to low reproductive the ability to monitor reproductive processes. success in recent years. Research needs include: Specific areas that warrant research are: methods understanding optimal body condition and to diagnose and monitor pregnancy, including nutritional needs for cub production; determining points of pregnancy failure; characterization of the influence of environmental contaminants on ovarian dynamics, including the stimulus required reproductive processes; identifying exogenous for ovulation; evaluation of steroid hormones and/or endogenous cues for regulation of and biosynthesis pathways; investigation of emergence from embryonic diapause; evaluating temporal trends in non-steroid hormones, and; housing and/or management strategies, including examination of biomarkers of metabolism and their relationships to reproduction. light and noise pollution, on reproductive behavior and cub production; evaluating the genetic 2. Identify factors impacting reproductive relatedness of individuals in zoos, and; developing success: It is generally unknown why some zoo and utilizing assisted reproductive technologies managed bears produce cubs and others do not, (ART) to maintain a research population and to despite exhibiting seemingly normal copulatory preserve valuable genetics. PRBC Masterplan 2022 | 21
REPRODUCTION 3. Assess reproductive anatomy and gamete biology: There is limited data on the basic anatomy of polar bear reproductive systems and pathologies that may impact reproductive processes. Immobilizations and necropsies provide opportunities to visualize and evaluate reproductive tracts, assess pathologies, collect and cryopreserve gametes to preserve valuable genetic material, and preserve tissues collected post-mortem. Reproductive studies currently underway or not yet published Non-invasive monitoring: Fecal steroid metabolite changes associated with sexual maturation (CREW, manuscript in prep); Dehydroepiandrosterone (DHEAS) quantification in feces collected from both zoo and wild bears (Brandhuber, U of Alaska Fairbanks; quantification of testosterone concentrations in group- housed vs. solo housed male polar bears (McCart, York University); PGFM quantification in parturient vs. non- parturient bears (CREW). Pregnancy diagnosis: Investigation into specific fecal proteins as biomarkers of pregnancy using sequential window acquisition of all theoretical ion fragments (SWATH; CREW); fecal volatile organic compound (VOC) analysis (collaboration between CREW and Dr. Wilson at University of Saskatchewan); fecal metabolomics profiling (collaboration between CREW and Cincinnati Children’s Hospital Medical Center) Researchers perform a fertility exam and artificial insemination procedure. Vaginal endoscopy allows Serum hormone analysis: Quantification of Anti-Mullerian visualization of the cervix. Photo by Henry Vilas Zoo. hormone (AMH) concentrations by sex, season, age, and fertility status (Tompros/CREW); development of a multi- plex serum panel to measure leptin, prolactin, FSH, LH, extenders (CREW, Toronto Zoo); laparoscopy and kisspeptin, melatonin, and Vitamin D in serum banked from zoo bears (Wojtusik/CREW). ultrasonography of the female polar bear (Justine O’Brien, SeaWorld & Busch Gardens Reproductive Identifying factors impacting reproduction: Long-term Research Center (SWBGRRC), Todd Robeck (SWBGRRC), effects of contraception on reproduction in polar bears and Dean Hendrickson (Colorado State); vaginal (CREW, manuscript under review); nutrition and body endoscopy, endocrine data (paired fecal and urine), weight during pregnancy (Toronto Zoo, in process). and AI (Justine O’Brien, Karen Steinman (SWBGRRC), Physiological assessments of reproductive systems: and CREW); histopathology of reproductive tracts Semen collection and cryopreservation, both at collected post-mortem (Agnew & Shellabarger); physical examinations and post-mortem/post- assessment of prevalence of perivulvar dermatitis in castration (CREW, Toronto Zoo); evaluation of semen zoo bears (Shellabarger). 22 | PRBC Masterplan 2022
References Anderson, C.J.R., Lobo, N.D.V., Roth, J.D., and Waterman, Curry, E., Safayi, S., Meyerson, R., and Roth, T.L. (2015). J.M. (2010). Computer-aided photo-identification Reproductive trends of captive polar bears (Ursus system with an application to polar bears based maritimus) in North American zoos: a historical on whisker spot patterns. Journal of Mammalogy analysis. Journal of Zoo and Aquarium Research 91(6):1350–1359. 3:99-106. Atwood, T.C., Colleen Duncan, C., Patyk, K.A., Nol, P., Curry, E., Skogen, M., and Roth, T.L. (2021). Evaluation of Rhyan, J., McCollum, M., McKinne, M.A., Ramey, A.M., an odour-detection dog for non-invasive pregnancy Cerqueira-Cézar, C.K., Kwok, O.C.H., Dubey, J.P., and diagnosis in polar bears (Ursus maritimus): Hennage, S. (2017). Environmental and behavioral Considerations for training sniffer dogs for biomedical changes may influence the exposure of an Arctic investigations in wildlife species. Journal of Zoo and apex predator to pathogens and contaminants. Aquarium Research 9:1-7. Scientific Reports 7:13193. Curry, E., Stoops, M.A., and Roth, T.L. (2012). Non- Barnas, A.F., Felege, C.J., Rockwell, R.F., and Ellis-Felege, invasive detection of candidate pregnancy protein S.N. (2018). A pilot (less) study on the use of an biomarkers in the feces of captive polar bears (Ursus unmanned aircraft system for studying polar bears maritimus). Theriogenology 78:308-314. (Ursus maritimus). Polar Biology 41(5):1055-1062. Derocher, A.E., and Stirling, I. (1994). Age-specific Bissonnette, P. (2020). Adult polar bear behaviour: Using reproductive performance of female polar bears non-invasive techniques to assess social play. MSc (Ursus maritimus). Journal of Zoology 234:527–536. thesis, University of Manitoba, Canada. Durner, G.M., Douglas, D.C, Albeke, S.E., Whiteman, J.P., Bowen, L., Miles, A.K., Waters, S., Meyerson, R., Rode, K., Amstrup, S.C., Richardson, E.S., Wilson, R.R., and Ben- and Atwood, T. (2015). Gene transcription in polar David, M. (2017). Increased Arctic sea ice drift alters bears (Ursus maritimus) from disparate populations. adult female polar bear movements and energetics. Polar Biology DOI 10.1007/s00300-015-1705-0. Global Change Biology 23:3460-3473. Bryant, J., and Roth, T.L. (2018). Annual faecal Dutton, C.J. , Quinnell, M., Lindsay, R., DeLay, J., and glucocorticoid metabolite concentrations in Barker, I.K. (2009). Paraparesis in a polar bear (Ursus pregnant and pseudopregnant polar bears (Ursus maritimus) associated with West Nile virus infection. maritimus) in North American zoos. Journal of Zoo Journal of Zoo and Wildlife Medicine 40(3):568-71. and Aquarium Research 6(1):6–11. Fagre, A.C., Patyk, K.A., Nol, P., Atwood, T., Hueffer, K., Curry, E., and Roth, T.L. (2016). A rapid, minimally-invasive and Duncan, C. (2015). A review of infectious agents method of collecting semen from polar bears. in polar bears (Ursus maritimus) and their long- Proceedings of the International Embryo Transfer term ecological relevance EcoHealth DOI: 10.1007/ Society 42nd Annual Conference. Louisville, KY. s10393-015-1023-6. Curry, E., and Roth, T.L. (2017). A rapid method of semen Knott, K.K., Mastromonaco, G.F., Owen, M.A., and collection from polar bears immobilized with Kouba, A.J. (2017). Urinary profiles of progestin and medetomidine. Proceedings of the 22nd Biennial androgen metabolites in female polar bears during Society for Marine Mammalogy. Halifax, Nova Scotia. parturient and non-parturient cycles. Conservation Curry, E., Roth T.L., MacKinnon K.M., and Stoops, M.A. Physiology 5:1-12. (2012). Factors influencing annual fecal testosterone metabolite profiles in captive male polar bears (Ursus maritimus). Reproduction of Domestic Animals 47:222-225. PRBC Masterplan 2022 | 23
LaRue, M.A., Stapleton, S., Porter, C., Atkinson, S., Atwood, Owen, M.A., Pagano A.M., Wisdom, S.S., Kirschhoffer, T., Dyck, M., and Lecomte, N. (2015). Testing methods B., Bowles, A.E. and O’Neill, C. (2021). Estimating for using high‐resolution satellite imagery to monitor the audibility of industrial noise to denning polar bear abundance and distribution. Wildlife polar bears. The Journal of Wildlife Management Society Bulletin 39(4):772-779. 85(2):384-396. McKinney, M.A., Atwood, T.C., Pedro, S., and Peacock, E. (2017). Ecological change drives a decline in Pagano, A.M., Carnahan, A.M., Robbins, C.T., Owen, M.A., mercury concentrations in Southern Beaufort Sea Batson, T., Wagner, N., Cutting, A., Nicassio-Hiskey, N., polar bears. Environmental Science and Technology Hash, A., and Williams, T.M. (2018a). Energetic costs 51:7814-7822. of locomotion in bears: is plantigrade locomotion energetically economical? Journal of Experimental McKinney, M.A., Peacock, E., and Letcher, R.J. (2009). Sea Biology 221(12), DOI:p.jeb175372. ice-associated diet change increases the levels of Pagano, A.M., Cutting, A., Nicassio-Hiskey, N., Hash, A., chlorinated and brominated contaminants in polar and Williams, T.M. (2018b). Energetic costs of aquatic bears. Environmental Science and Technology locomotion in a subadult polar bear. Society for 43:4334-4339. Marine Mammalogy DOI: 10.1111/MMS.12556. Molnár P.K., Derocher, A.E., Klanjscek, T., and Lewis, M.A. Pagano, A.M., Durner, G.M., Amstrup, S.C., Simac, K.S., and (2011). Predicting climate change impacts on polar York, G.S. (2012). Long-distance swimming by polar bear litter size. Nature Communications 2:186. bears (Ursus maritimus) of the southern Beaufort Neuman-Lee, L.A., Terletzky, P.A., Atwood, T.C., Gese, Sea during years of extensive open water. Canadian E.M., Smith, G.D., Greenfield, S., Pettit, J., and French, Journal of Zoology 90:663-676.s S.S. (2017). Demographic and temporal variations Pagano, A.M., Robbins, C.T., Carnahan, T., Owen, in immunity and condition of polar bears (Ursus M.A., Batson, T., Wagner, N., Hash, A., Williams, maritimus) from the southern Beaufort Sea. Journal T.M. (2018c). Costs of locomotion in two large of Experimental Zoology: 327(5):333-346. plantigrade carnivores: polar bears and grizzly Obbard, M.E., Cattet, M.R.L., Howe, E.J., Middel, K.R., bears. Journal of Experimental Biology 221(12): Newton, E.J., Kolenosky, G.B., et al. (2016). Trends in https://doi.org/10.1242/jeb.175372 body condition in polar bears (Ursus maritimus) from Pagano, A.M., Rode, K.D., Cutting, A., Owen, M.A., Jensen, the Southern Hudson Bay subpopulation in relation S., Ware, J.V., Robbins, C.T., Durner, G.M., Atwood, to changes in sea ice. Arctic Science 2:15-32. T.C., Obbard, M.E., Middel, K.R., Thiemann, G.W., and Owen, M.A., and A. E. Bowles. (2011). In-air auditory Williams, T.M. (2017). Using tri-axial accelerometers psychophysics and the management of a threatened to identify wild polar bear behaviors. Endangered carnivore, the polar bear (Ursus maritimus). Species Research 32:19-33. International Journal of Comparative Psychology 24:244-254. Prop, J., Staverlokk, A., and Moe, B. (2020). Identifying individual polar bears at safe distances: A test with Owen, M.A., Swaisgood, R.R., Slocomb, C., Amstrup, captive animals. PLoS ONE 15(2): e0228991. S.C., Durner, G.M., Simac, K., and Pessier, A.P. Rode, K.D., Amstrup, S.C., and Regehr, E.V. (2010). (2015). An experimental investigation of chemical Reduced body size and cub recruitment in polar communication in the polar bear. Journal of Zoology bears associated with sea ice decline. Ecological 295:36-43. Applications 20:768-782.
You can also read